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Transcription, structure, and organoids translate time across the lifespan of humans and great apes

How the neural structures supporting human cognition developed and arose in evolution is an enduring question of interest. Yet, we still lack appropriate procedures to align ages across primates, and this lacuna has hindered progress in understanding the evolution of biological programs. We generate...

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Autores principales: Charvet, Christine J, Ofori, Kwadwo, Falcone, Carmen, Rigby Dames, Brier A
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10406161/
https://www.ncbi.nlm.nih.gov/pubmed/37554928
http://dx.doi.org/10.1093/pnasnexus/pgad230
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author Charvet, Christine J
Ofori, Kwadwo
Falcone, Carmen
Rigby Dames, Brier A
author_facet Charvet, Christine J
Ofori, Kwadwo
Falcone, Carmen
Rigby Dames, Brier A
author_sort Charvet, Christine J
collection PubMed
description How the neural structures supporting human cognition developed and arose in evolution is an enduring question of interest. Yet, we still lack appropriate procedures to align ages across primates, and this lacuna has hindered progress in understanding the evolution of biological programs. We generated a dataset of unprecedented size consisting of 573 time points from abrupt and gradual changes in behavior, anatomy, and transcription across human and 8 nonhuman primate species. We included time points from diverse human populations to capture within-species variation in the generation of cross-species age alignments. We also extracted corresponding ages from organoids. The identification of corresponding ages across the lifespan of 8 primate species, including apes (e.g., orangutans, gorillas) and monkeys (i.e., marmosets, macaques), reveals that some biological pathways are extended in humans compared with some nonhuman primates. Notably, the human lifespan is unusually extended relative to studied nonhuman primates demonstrating that very old age is a phase of life in humans that does not map to other studied primate species. More generally, our work prompts a reevaluation in the choice of a model system to understand aging given very old age in humans is a period of life without a clear counterpart in great apes.
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spelling pubmed-104061612023-08-08 Transcription, structure, and organoids translate time across the lifespan of humans and great apes Charvet, Christine J Ofori, Kwadwo Falcone, Carmen Rigby Dames, Brier A PNAS Nexus Biological, Health, and Medical Sciences How the neural structures supporting human cognition developed and arose in evolution is an enduring question of interest. Yet, we still lack appropriate procedures to align ages across primates, and this lacuna has hindered progress in understanding the evolution of biological programs. We generated a dataset of unprecedented size consisting of 573 time points from abrupt and gradual changes in behavior, anatomy, and transcription across human and 8 nonhuman primate species. We included time points from diverse human populations to capture within-species variation in the generation of cross-species age alignments. We also extracted corresponding ages from organoids. The identification of corresponding ages across the lifespan of 8 primate species, including apes (e.g., orangutans, gorillas) and monkeys (i.e., marmosets, macaques), reveals that some biological pathways are extended in humans compared with some nonhuman primates. Notably, the human lifespan is unusually extended relative to studied nonhuman primates demonstrating that very old age is a phase of life in humans that does not map to other studied primate species. More generally, our work prompts a reevaluation in the choice of a model system to understand aging given very old age in humans is a period of life without a clear counterpart in great apes. Oxford University Press 2023-07-20 /pmc/articles/PMC10406161/ /pubmed/37554928 http://dx.doi.org/10.1093/pnasnexus/pgad230 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of National Academy of Sciences. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Biological, Health, and Medical Sciences
Charvet, Christine J
Ofori, Kwadwo
Falcone, Carmen
Rigby Dames, Brier A
Transcription, structure, and organoids translate time across the lifespan of humans and great apes
title Transcription, structure, and organoids translate time across the lifespan of humans and great apes
title_full Transcription, structure, and organoids translate time across the lifespan of humans and great apes
title_fullStr Transcription, structure, and organoids translate time across the lifespan of humans and great apes
title_full_unstemmed Transcription, structure, and organoids translate time across the lifespan of humans and great apes
title_short Transcription, structure, and organoids translate time across the lifespan of humans and great apes
title_sort transcription, structure, and organoids translate time across the lifespan of humans and great apes
topic Biological, Health, and Medical Sciences
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10406161/
https://www.ncbi.nlm.nih.gov/pubmed/37554928
http://dx.doi.org/10.1093/pnasnexus/pgad230
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